The current status of geriatric oncology in India

Geriatric oncology in India is relatively new. The number of older persons with cancer is increasing exponentially; at our institution, 34% of patients registered are 60 years and over. Apart from the Tata Memorial Hospital in Mumbai, there are currently no other Indian centers that have a dedicated geriatric oncology unit. Geriatric assessments (GAs) are done sporadically, and older patients with cancer are usually assessed and treated based on clinical judgement. Challenges to increasing the uptake of GA include a lack of training/time/interest or knowledge of the importance of the GA. Other challenges include a lack of trained personnel with expertise in geriatric oncology, and a paucity of research studies that seek to advance the outcomes in older Indian patients with cancer. We anticipate that over the next 10 years, along with the inevitable increase in the number of older persons with cancer in India, there will be a commensurate increase in the number of skilled personnel to care for them. Key goals for the future include increased research output, increased number of dedicated geriatric oncology units across the country, India-specific geriatric oncology guidelines, geriatric oncology training programs, and a focus on collaborative work across India and with global partners. In this narrative review, we provide a broad overview of the status of geriatric oncology in India, along with a description of the work done at our center. We hope to spark interest and provide inspiration to readers to consider developing geriatric oncology services in other settings.


Introduction
Geriatric oncology in India is in its infancy.The majority of older Indian patients with cancer are not evaluated systematically with a validated geriatric assessment (GA), but rather are assessed using clinical judgement.Due to a severe shortage of persons skilled in geriatric oncology, and the lack of dedicated geriatric oncology units both in major academic centers as well as in corporate hospitals and private practices in India, the care provided to older Indian patients with cancer is likely to be sub-optimal [1].Besides, several GA tools and scales that were developed in the West are not suitable for some older Indian patients, due to differences in cultural experiences, illiteracy, and varying life expectancies [2].
The functional status is a measure of the ability of an individual to perform tasks that maintain independence [3].This functional status declines progressively with age, making older individuals vulnerable to stressors and rendering some incapable of living independently, functionally and socially [4].There is heterogeneity in the ageing process, which further contributes to the complexity of treatment decisions.These factors result in age-related variations in treatment patterns and outcomes, potentially culminating in under-or overtreatment, which can influence both the risks of treatment toxicity, and survival [5].Though the Eastern Cooperative Oncology Group (ECOG) performance status (PS), which is the traditional method used by oncologists to evaluate functional status globally, has been found to correlate moderately well with vulnerabilities in various geriatric domains, it cannot replace a formal GA [6].Despite the broad scope of geriatric oncology, only a few Indian centers offer a formal geriatric oncology service, or the ability to provide specialised care to an older person with cancer.
There are myriad other issues plaguing geriatric oncology in India, including a lack of teaching programs, almost no research studies that either include older persons with cancer or focus on issues important to older patients with cancer, and a lack of an inter-institutional and pan-India collaborative effort to advance the care of older Indian patients with cancer.Many of these issues are not unique to India, but are global phenomena.We explore the current status of geriatric oncology in India, the challenges, strengths and opportunities and suggest the key focus areas over the course of the next decade.Through this review article, we hope to inspire at least some readers to build up geriatric oncology services at their clinics, and establish centers of excellence in geriatric oncology at various institutions across India.

Epidemiology of older adults in India
In 2010, 524 million individuals globally were aged 65 years or older.By the year 2050, the World Health Organisation has predicted that 1.5 billion people will be 65 years or older [7].Nearly 80% of these older individuals will be living in low-and middle-income countries [8].This will have a tremendous impact on the global cancer burden.India is also witnessing a demographic transition.In 2011, older persons constituted 8.6% of India's total population, equalling 103 million [9].This proportion is expected to increase exponentially and is projected to reach 19.5% in 2050, equalling 319 million people.The proportion of the oldest-old, i.e., those aged 75 years and over, is projected to rise by 340% [10,11].
Advancing age is a risk factor for the development of malignancy, with persons over 65 years accounting for 60% of newly diagnosed malignancies and 70% of cancer deaths.These mainly include cancers of the breast, lung, prostate, cervix, esophagus and ovary [12].Globally, there are geographic and economic factors that affect the number of older people living with and surviving cancer, but data show a common trend that a large proportion of people with cancer are older [13,14].The Indian Council of Medical Research National Cancer Registry Program estimates that the number of cancer diagnoses will increase from 1.39 million in 2020 to 1.57 million by 2050 [15].Thus, the number of older persons with cancer is expected to rise exponentially in India over the next few years.Data from our hospital-based registry at the Tata Memorial Hospital in Mumbai revealed that between January 2019 and December 2021, there were 29,768 patients with cancer registered who were over 60 years old among the total pool of 87,101 newly registered patients, i.e., 34.2% of the total number of patients with cancer registered at our institute were 60 years or older [unpublished data].

Uptake of the GA in India
We conducted a survey among 100 physicians to assess the situation at the ground level regarding the extent of knowledge and practice of GA in India [16].Although 99% of respondents cared for older patients with cancer, with 87% caring for 10 or more per week, 51% did not routinely perform a GA.Almost 70% of the survey participants relied on 'intuition' to formulate the management plan; less than 10% used validated tools.Additionally, 44% were unaware of the American Society of Clinical Oncology (ASCO) geriatric oncology guidelines.Barriers to performing the GA routinely included lack of time, staff, awareness, resources and space, and an uncertainty regarding which GA tools to use.The results of our survey underlined the need to devise a tailored GA tool in India for screening, evaluation, and management in limited resource settings [16].

Oncologists' perceptions of the need for assessing individual domains in the GA and worthwhile outcomes
We conducted a follow-up survey among 234 healthcare professionals (71% medical oncologists, 11.7% radiation oncologists, and 10.7% surgical oncologists) to understand the perceived relative importance of assessing various GA domains [17].Over 99% participants thought that it was important to assess comorbidities, polypharmacy, medications, drug interactions and social support.Over 98% thought it important to assess function, falls, and quality of life (QoL).Approximately 97% thought that assessment of nutrition and cognition was important, while 93.6% thought that psychological evaluation was important.Regarding the goals of performing a GA, 90% hoped that it would lead to an improvement in QoL, 65.6% desired a decrease in toxicity, and 42.9% wished for survival prolongation.Regarding the relative importance of a decrease in treatment toxicity or improvement in QoL versus survival prolongation in older patients with cancer, 62.6% found toxicity + QoL more important, 36.9% found them as important and only 0.5% respondents felt that decreasing toxicity and improving QoL were less important than prolonging survival [17].

Defining the age-cutoff for 'old'
The answer to the question, 'How old is old?' varies based on multiple factors.For an individual, the factors are myriad; however, at the population level, the answer is straightforward and based on life expectancy and retirement age [18].The International Society of Geriatric Oncology (SIOG) defines this age as 70 years, while the ASCO recommendations are for persons aged 65 years and older.When we started the geriatric oncology clinic at the Tata Memorial Hospital (TMH), in Mumbai, India, we evaluated patients aged >65 years based on the ASCO guidelines [19].We later realised that the age cut-off to define 'old age' varies across cultures, and that using the age cutoff established by an American organisation was not appropriate for Indian patients.The average life expectancy in India is 70.4 years overall; 71.8 years for women, and 69.2 years for men [20], which is much lower than that of people living in Japan (85 years) or the United States (79 years).In Japan, the age cut-off for the geriatric population is considered to be 75 years, while in India, according to the National Program for Health Care of the Elderly (NPHCE) [21] established by the Government of India, an older person is defined as anyone who is 60 years or older.Hence the age cut-off in our geriatric oncology clinic was changed to 60 years [22].This age cut-off is followed by other Indian clinicians as well [23,24].

Geriatric oncology service at the Tata Memorial Hospital
TMH has a well-established geriatric oncology multidisciplinary service for patients aged 60 years and above with cancer.Starting on June 15, 2018, as a 1-day-a-week outpatient clinic, the service now functions daily, both for outpatients and inpatient consultations.Our goal is to perform detailed GAs and provide multidisciplinary, patient-specific care plans (Figure 1).In addition, we also run an academic teaching program and are attempting to bridge the research gap.The clinic is run by two medical oncologists; other members include a geriatric oncology fellow (trainee), senior residents, and patient coordinators.This multidisciplinary clinic also comprises clinical pharmacologists, geriatricians, onco-psychologists, physiotherapists, occupational therapists, dieticians, and social workers.Although initial referrals to our clinic were sparse, these have increased exponentially over time (except for the brief period when we closed the clinic from Apr to Jun 2020 during the peak of the COVID-19 pandemic), and currently, we assess approximately 20-30 patients a week.Between Jun 15, 2018, and May 12, 2023, we have assessed 2,322 patients (Figure 2).

Overall assessment
All patients referred to our geriatric oncology clinic undergo a detailed evaluation for the presence of vulnerabilities in various geriatric nononcologic domains and caregiver burden.Patients are evaluated for geriatric syndromes (constipation, insomnia, lower urinary tract symptoms, urinary incontinence, osteoporosis, pressure sores), visual and hearing impairment, voice, and oral health.We assess chemotherapy toxicity risk using the Cancer and Aging Research Group (CARG) tool and estimate the non-oncologic life expectancy using ePrognosis.We also evaluate financial toxicity, and overall QoL (Table 1).

Non-oncologic domains
The various GA tools used at our clinic, along with the cut-offs have been provided in Table 1.

Blood tests
The patient's baseline haemoglobin, creatinine, albumin and sodium are noted, and the estimated glomerular filtration rate (eGFR) is calculated for all patients.Additionally, we determine the patient's neutrophil-lymphocyte ratio (NLR) considering it a prognostic inflammatory marker in older patients with cancer.

Patients' and caregivers' goals of therapy
The patient's perspective regarding the intent of therapy (curative/palliative) and the patient's expectations from treatment and the patients'/ primary caregivers' wishes regarding disclosure about the diagnosis/prognosis are discussed, and integrated into the care plan.

Appropriateness of GA tools for older Indian adults
The GA has been developed in a predominantly western urban cohort of patients, and multiple aspects are culturally inappropriate for our Indian patients [2].The problems with individual assessment using tools, such as instrumental activities of daily living (IADL) (roles and responsibilities within family vary diversely), mini-mental status examination (MMSE) (literacy, relocation to Mumbai for treatment, unawareness of dates according to the Gregorian calendar), mini-nutritional assessment (MNA) (lack of access to a weighing scale, thin body habitus), a cumulative illness rating scale for geriatrics (CIRS-G) (lack of strong primary healthcare systems, so no robust diagnosis and therapy of comorbidities), geriatric depression scale (GDS) and generalised anxiety disorder assessment-7 (GAD7) (culturally inappropriate questions) are prevalent.We have found that multiple portions of the GA are culturally inappropriate and could not be analysed or led to unreliable results [2].The first step in tackling this issue was taken by Banerjee et al [54], who developed a short-35-item screening tool that would be appropriate for Indian patients.Further, they also identified suitable cut-off scores that correlated with survival, which could help streamline care in a resource-limited setting [55].By reconciling the cultural differences and establishing a GA directed at Indian patients with cancer, we hope to be able to provide better service to our patients.
In addition to socio-cultural differences, phenotypic diversity cannot be ignored.The normal range of the body mass index (BMI) for the Asian population is lower as compared to that in western countries [56].We identified that the cut-off TUG score of 12 seconds [19] was not as sensitive, and a lower cut-off score of 10 seconds was more appropriate for older Indian patients with cancer [57].

Prevalence of non-oncologic vulnerabilities in older persons with cancer in India
In our geriatric oncology clinic at TMH, the median time to perform a GA is 50 minutes (IQR, 40-61) [58].Despite the time-consuming process, we found that the GA was very valuable in detecting geriatric vulnerabilities.About 98% of our patients had vulnerabilities in at least one geriatric domain.The abnormalities noted were in the domains of comorbidities (79%), fatigue (77%), nutrition (65%), function and falls (52%), mood (32%), and cognition (18%) [58].We also observed that 55% of the patients had polypharmacy, 80% were on potentially inappropriate medications (PIM), and nearly 23% were taking alternative medications (ayurvedic/naturopathic/homeopathic) [59].Almost 60% needed referrals to a physiotherapist and occupational therapist, 69% required dietary intervention and 29% required evaluation and management by a psychologist/counsellor.

Impact of the GA on the systemic therapy plan
Globally, it is well recognised that systematic evaluation of older patients with cancer with a GA is valuable and leads to better treatment choices, lowers toxicity and improves communication.However, conducting the GA is time-and labor-intensive, and resources are limited at most centers in India.At our institution, the GA led to a change in cancer-directed systemic therapy plan in 38.7% of cases, with the commonest change being treatment de-intensification in 32.1% of patients [60].Thus, a significant proportion of our older patients with cancer are over-treated in cases where a GA is not performed.

Status of research in geriatric oncology in India
Due to the heterogeneous population and lack of data from older Indian patients with cancer, we generally need to extrapolate the results from studies done in other populations [63].Broadly, we envision that the most impactful geriatric oncology research in India would include epidemiologic research to understand the demographic profile and various other epidemiologic parameters; tool validation research to test the appropriateness of assessment tools; implementation research to discover and test methods to increase the uptake/streamline or improve the efficiency of the GA; observational studies to understand the various aspects of geriatric oncology; therapeutic research aimed either at testing, cancer-directed therapy or treatment-related toxicities; and patient-centric research to understand and improve the experiences/perspectives/challenges faced by patients/caregivers (Table 2).A major challenge to conducting geriatric oncology research in India is the lack of collaboration.A limiting factor is the lack of centers that have geriatric oncology units and clinicians who have expertise in geriatric oncology.We have attempted to address this issue by forming a group of like-minded clinicians from various centers across India who have an interest in geriatric oncology.Several initiatives have been taken in this group to bridge the knowledge and research gap in geriatric oncology in India, some of which have been described in Table 2.

Patient and caregiver support groups
Addressing the supportive care needs of an increasing number of older patients with cancer and their caregivers requires innovative strategies and delivery methods.Support groups bring together people who are going through or have gone through similar experiences.Online support groups are social spaces where people with shared interests can gain and share information and support.Spurred on by the COVID-19 pandemic and the increasing need for additional counselling/support/advice by patients and caregivers, in May 2022 we started an online support group for patients and caregivers of older patients with cancer.This is conducted with the help of a non-governmental organisation, and has been held on a virtual platform successfully every month.Along with patients and caregivers sharing their views and experiences, they are also educated regarding the importance of maintaining the patients' functionality, nutrition, cognitive capacity and mood.

Action points for the next decade
In the coming decade, there will be an exponential increase in the number of older persons with cancer.In order to provide optimal support for these older and often frail patients, our focus will be on five high-impact areas, outlined in Table 3.

Conclusion
There is a need for awareness of geriatric oncology among practicing physicians who care for older patients with cancer.Only a few institutes in India provide specialised geriatric oncology services.Recognising the importance and implementing such a service to optimally manage this vulnerable population is an urgent necessity.At the Tata Memorial Hospital in Mumbai, we have established a comprehensive multidisciplinary geriatric oncology service and are attempting to fill the gap in terms of providing specialised care to older patients with cancer, designing and implementing research studies that focus on this cohort of patients, and disseminating high-quality education to students and colleagues.Since the clinic was established in June 2018, we have accomplished a lot in terms of clinical service, education and research; however, much more needs to be done.More physicians, oncologists, geriatricians, and nursing staff need to be trained to perform GAs, interpret the results, and prepare tailored care plans.There is a need to develop and validate suitable and culturally appropriate tools to assess older Indian patients with cancer.-GA is prognostic for survival in older Indian patients with cancer.
-GA is prognostic even in patients thought to be the fittest, i.e., PS 0 and 1.
-GA must be done in all older Indian patients planned for cancer-directed therapy.
(Continued) -83.3% had received at least one dose of the COVID-19 vaccine.
-Factors associated with COVID-19 vaccine uptake: education, marital status, geographic zone and primary tumour site.
-Fewer than one in 100 older Indian persons with cancer receive routine immunisation with influenza and pneumococcal vaccines.
-The uptake of COVID-19 vaccination in older Indian persons with cancer is over 80% -Similar strategies as those used to increase COVID-19 vaccination should be employed to increase the uptake of routine vaccinations.
- -12.4% had to borrow money, 4.3% had taken a loan, 2.6% sold their assets for the purposes of treatment.
-Moderate-severe financial burden on COST-FACIT present in 33.1%, whereas 66.9% experienced no or mild burden.
-   There should be specialists who are trained in the assessment and care of older patients with cancer at every institution and clinic that manages older persons with cancer.
• Robust training programs to provide education in the principles and practice of geriatric oncology • Ongoing and frequent hands-on workshops and webinars Inter-instutional collaboration To establish an inter-institutional collaborative network of healthcare professionals for knowledge-sharing, collaborative research and other multicentric activities.
• To establish and register the Geriatric Oncology Society of India.
• Hold monthly meetings online • Organise an annual meeting/conference to decide the purpose, planned work and manifesto of the society.• Overarching goal will be to enhance the quality of service, education, and geriatric oncology research across multiple institutions in India Multicentric research studies To generate evidence that answers the unique issues of older Indian patients with cancer.
• Establish a group of like-minded researchers within the collaborative oncology network • Build a clinical trials wing within the group, and establish the necessary manpower and infrastructure to conduct high-quality research studies.• Brainstorm regarding the top research priorities, and decide the most important focus areas.• Apply to various funding agencies for the top projects.

India-specific geriatric oncology guidelines
To establish a set of minimum and optimal guidelines to streamline the assessment and care of older Indian patients with cancer • In order for these guidelines to be relevant and applicable to older Indian patients with cancer, we will need to: • Modify the existing global guidelines, and/or • Generate new culturally appropriate and country specific tools for assessment, and interventions.• These guidelines will have to be updated on a regular basis, perhaps every 2 to 3 years.

Figure 1 .
Figure 1.The process of evaluation and assessment in the geriatric oncology at the Tata Memorial Hospital in Mumbai, India.

Figure 2 .
Figure 2. The progressive increase in the number of older patients with cancer evaluated monthly in the geriatric oncology clinic at the Tata Memorial Hospital (Mumbai, India) since inception on June 15, 2018.
Acronyms: CARG = Cancer and Ageing Research Group; TUG = Timed Up and Go test; PIM = Potentially inappropriate medicines; GA = Geriatric assessment; QoL = Quality of life; ECOG PS = Eastern Cooperative Oncology Group; PS = performance status; AUC = Area under the curve; CI = Confidence interval; OS = Overall survival; HR = Hazard ratio; COST-FACIT = COmprehensive Score for financial Toxicity-Functional Assessment of Chronic Illness Therapy; OR = Odds ratio; GFR = Glomerular filtration rate; IQR = Interquartile range; NSCLC = Non-small-cell lung cancer; HNSCC = Head and neck squamous cell carcinoma; IQR = Interquartile range; CI = Confidence interval (Continued)

Table 1 . Details of the tools used, assessments performed and questionnaires administered as a part of the GA at the Tata Memorial Hospital (Mumbai, India).
'Maintaining purpose' scale and 'Family support' item indicates a high level of functioning; higher scores for 'Mobility', 'Worries about others', 'Future worries', 'Burden of illness,' and 'Joint stiffness' indicate a poor QoL

Table 1 . Details of the tools used, assessments performed and questionnaires administered as a part of the GA at the Tata Memorial Hospital (Mumbai, India).
[52]de 1); 1-13: moderate impact (grade 2); 0: high impact (grade 3))Consumer financial protection bureau financial well-being scale[52]Range: 0-100 points; Lower scores represent worse financial well-being Patients' and caregivers' viewpoint regarding disclosure 'Does the patient/caregiver want the treating team to disclose and discuss the diagnosis and prognosis?'Based on the patients' and caregivers' viewpoints, the results of the GA, the curability/treatability of the cancer and the potential toxicity of the therapy, a discussion occurs Patients' expectations from treatment If curative: Complete cure/symptom control/improvement in present status/improved QoL or prolongation of life If palliative: Improved QoL/prolongation of life/immediate symptom relief Blood tests eGFR Based on the kidney function, a decision will be taken NLR NLR <3.4 = Poor prognosis Vaccination status Uptake of pneumococcal, influenza, and COVID-19 vaccines If not received, patients are advised these vaccines *Risk of grade 3 or higher toxicity The Department of Medical Oncology at the Tata Memorial Hospital runs a 1-year geriatric oncology fellowship training program[61].The program admits doctors trained in Internal Medicine, Geriatric Medicine, and Medical Oncology.The fellow undergoes rigorous training in patient assessment, care-plan development, academic learning, and research protocol development and implementation.The department also conducts Geriatric Oncology workshops at least twice a year to train oncologists and primary care physicians.The goal of such continuous medical education includes spreading awareness of geriatric oncology, imparting education regarding the principles of geriatric oncology, and training for performing GAs for older patients with cancer.The Tata Memorial Center has also partnered with SIOG to conduct an annual advanced course in geriatric oncology[62].

Table 2 . Some of the research studies (completed, ongoing and planned) to bridge the knowledge gap of geriatric oncology in India.
*Collaborative multicentric study